Abstract. The renal arteries of 89 healthy full-term infants were examined using duplex Doppler ultrasonography to establish a normal range for renal blood flow ...
1991, The British Journal of Radiology, 64, 413-416
Doppler ultrasound studies in renal arteries of normal newborn babies By A. C. Lamont, FRCR, H. S. Hall, J . R. Thompson, PhD and D. H. Evans, PhD, FlnstP, FIPSM Department of Radiology, Leicester Royal Infirmary, Leicester LE5 1WW, UK
(Received November 1990 and in revised form December 1990) Keywords: Renal artery, Doppler, Neonate
Abstract. The renal arteries of 89 healthy full-term infants were examined using duplex Doppler ultrasonography to establish a normal range for renal blood flow velocity in the first 3 days of life. In the first 24 h a wide range of renal blood flow velocities was noted with a statistically significant decrease in Pourcelot's index over the next 2 days.
Duplex Doppler ultrasound is a simple means of measuring blood flow in human neonates, and the cardiac circulation has been extensively studied (Wilde, 1989). Arterial studies have been confined mainly to the cerebral circulation (Evans et al, 1988; Levene, 1988). The study of blood flow velocity waveforms in the renal arteries of adults (Dubbins, 1986) and children (Keller, 1989; Wong et al, 1989) with Doppler ultrasound has proved most useful in kidney transplants (Slovis et al, 1984; Murphy et al, 1987; Ubhi et al, 1987; Stringer et al, 1989). The changing Doppler pattern in the first few days of life has been described in the cerebral arteries (Archer et al, 1985; Drayton & Skidmore, 1986; Evans et al, 1988), the carotid arteries (Deeg & Rupprecht, 1988) and the superior mesenteric artery (Van Bel et al, 1990), but the changing pattern of neonatal renal blood flow, although previously investigated in animals, has not yet been established in humans. The aim of this study was to find the normal range of renal arterial blood flow velocities in the first 3 days of life. Methods Prior approval for the study was obtained from the Leicester District Ethical Committee and signed consent was obtained. All examinations were carried out in the presence of at least one parent. Pulsed Doppler recordings obtained from the renal arteries using the L558, 5 MHz linear transducer of an Acuson model 128 ultrasound scanner were made in digital form on magnetic tape. A minimum of five consecutive wave forms were collected and stored for processing. In order to eliminate possible adverse effects of insonation of the neonatal renal artery and surrounding tissues, the output power of the Acuson scanner was pre-set to "low". At this setting the worst-case spatial Address for correspondence: Department of Radiology, Leicester Royal Infirmary, Leicester LEI 5WW, UK. Vol. 64, No. 761
peak temporal average (SPTA) intensity is 150 mW/cm2 and the in situ value 34 mW/cm2 (data from Acuson, 1989). The maximum exposure time for each kidney was 7.5 min, which is well within accepted safety limits (Evans et al, 1989). The renal artery arises from the aorta at an angle 0° (90° to 45°). Therefore the kidney was first imaged longitudinally and 6° noted. The transducer was then rotated through 90° and angled cephalad by 9°, so that a transverse image of the kidney was seen with the renal artery vertically displayed and blood flow was directly towards the transducer. The Doppler sample area was positioned close to the hilum of the kidney. Adjustments were made to give a clear signal using both visual and auditory information and compensation was made for respiratory movement of the kidney (Fig. 1). The studies were performed in a warm room with the infant relaxed, either asleep or eyes open with no gross movements (Prechtl & Beintema, 1964). The babies were wrapped in a small blanket, flank exposed, and lay on their sides in a cot or in their mothers' arms. Two methods of extracting information from the Doppler signals were considered: analysis of the maximum frequency envelope (MFE) and analysis of the intensity weighted mean signal (IWM). The MFE was chosen for this study because of its greater immunity to noise. It was defined using a fast Fourier transfer analyser coupled to a computer (Gibbons et al, 1981; Schlindwein et al, 1988), and calibrated in terms of velocity using the Doppler equation. The Doppler signals were analysed for: (1) Peak systolic maximum flow velocity (PSMFV) in cm/s. (2) End-diastolic maximum flow velocity (EDMFV) in cm/s. (3) Pourcelot's pulsatility index (PI) was calculated according to the formula PI = (S—D)/S where 5 and D are the maximum and minimum values of the maximum velocity envelope. PSMFV, EDMFV and PI were plotted against the post-delivery age, Apgar score and body weight. 413
A. C. Lamont, H. S. Hall, J. R. Thompson and D. H. Evans
AGE OF CHILD IN HOURS
Figure 1. Renal arterial Doppler signal with duplex image showing the hilum of the kidney in tilted transverse section. The Doppler probe can be seen positioned over the renal artery, adjacent to the renal vein, with arterial blood flow directed towards the transducer.
Figure 3. End-diastolic flow velocity plotted against the age of the infant in hours. The fitted trend is shown. Right kidney ( • ) ; left kidney (O).
Data were analysed using a bivariate linear regression, which allows for the correlation between values recorded on the right and left kidneys of the same infant at the same session, with modification to allow for missing data (Rosner, 1984).
No information was obtained from 14 infants, not included in the study, owing to a temporary technical fault in the recording system and three further infants with congenital anomalies or pathological changes were excluded (two cases of unilateral hydronephrosis, and one duplex kidney). In these cases the parents and attending medical officer were informed.
Patients During a 10-day period in February 1989 at the Leicester Royal Infirmary Maternity Hospital, 89 consecutive normal newborn babies (gestational age between 39 and 42 weeks) were examined between 1 and 3 days after birth. Eight infants were scanned on two occasions and two were scanned three times. Both kidneys were recorded on 77 occasions and only one kidney recorded in 17 instances. Satisfactory Doppler studies were obtained from a total of 171 kidneys. In only seven renal arteries were fewer than five consecutive Doppler wave forms obtained owing to excessive renal movement, and it was noted that in these cases the PI was not noticeably different from the contralateral side. They were therefore included in the study.
Results
The PSMFVs showed no change over the period of study (p = 0.73) (see Fig. 2) and the average was found to be 21.2 cm/s (standard error (SE) 0.64 cm/s) with a standard deviation (SD) of 7.0 cm/s. Correlation between PSMFVs of the right and left kidneys was 0.52. The EDMFV showed a rise over the period of the study (p = 0.007); the regression line was given by EDMFV = 2.94 + 0.0399 age in hours, where age ranged up to 60 h in this sample. Standard errors of these two coefficients were 0.33 and 0.014 (see Fig. 3). The correlation between the right and left kidneys was 0.62 and SD about the best-fit line was 0.787. Pourcelot's index showed a constant fall over the period of the study, mirroring the EDMFV (p = 0.001); the regression line was given by PI = 1.861—0.00221 age, where the SE of these two coefficients were 0.15 and 0.00065 (see Fig. 4). Correlation between left and right side was 0.74 and SD about the best-fit line was 0.100. Figure 5 shows the PI of 10 infants scanned on more than one occasion (left and right kidneys averaged), which confirms the general trend seen on the patients studied only once. Birth weights and Apgar scores of the infants were also recorded, but no correlation was seen with the PI. Discussion
AGE OF CHILD IN HOURS
Figure 2. Peak systolic flow velocity plotted against age of infant in hours. The fitted trend is shown. Right kidney ( • ) ; left kidney «>)•
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In order to estimate absolute renal blood flow using Doppler, a precise measurement of the internal vessel diameter is critical. Any errors in calculation of the cross-section are doubled. This is the weakest link in the estimation of volumetric flow (Gill, 1985) and we felt The British Journal of Radiology, May 199 J
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that direct measurements of the small neonatal vessels in our study were too inaccurate to be relied on. The measurement of PI, although it has some limitations, has been shown to have value for prediction of problems in the cerebral circulation of term infants (Archer et al, 1986). The rapid turnover of otherwise healthy patients at this hospital meant that a longitudinal study of normalterm babies was not possible, most being discharged within 1 day. Great care was taken to ensure that only healthy full-term babies were studied and infants available beyond the initial 24 h period remained in hospital for maternal health or other social reasons. Although this study has the disadvantage of being largely crosssectional, our trends are comparable to cerebral arterial studies in term infants by Drayton (Drayton & Skidmore, 1987). We observed a wide spread of mean maximum renal arterial blood flow velocities at all ages. However, factors such as the varying state of arousal of the infants or the time since the last meal may have contributed to this. Correlation between right and left renal arteries was 0.74 suggesting that the range reflects biological distribution. Mean systolic velocity remained constant over the 60 h observation period. However, diastolic velocity—and presumably, therefore, the mean renal arterial velocity—progressively increased. The mechanism for increase in renal arterial velocity is uncertain. Blood pressure, low at birth but progressively rising on average by 15 mmHg in the first 10 days of life (Bucci et al, 1972), has some effect but this is much smaller than observed changes. The PI was observed to fall with time, which may indicate localized renovascular dilatation or shunting distal to the Doppler sample site (Drayton & Skidmore, 1986, 1987; Wright et al, 1988). It is most likely that these circulatory changes can be explained by generalized physiological alterations within the renal vasculature and that the concomitant fall in PI could indicate distal renal vasodilatation. However, the effect of closure of a patent ductus arteriosis could
possibly cause a decrease in Pf, although none of the infants in this study had clinical evidence of PDA. This point was previously addressed in the cerebral arteries (Gentile et al, 1981; Perlman & Volpe, 1981). In utero studies on fetal lambs have shown low renal blood flow associated with the output of a large volume of dilute urine, possibly due to reduced tubular sodium reabsorption (Robillard et al, 1981). At birth the kidneys are, even in full-term infants, histologically immature and subsequent maturation is relatively slow (Alexander & Nixon, 1961). They take over from the placenta primary regulation of fluids, electrolytes and excretion of potentially toxic substances. Concentrations of urine must be established almost immediately after birth to prevent excess fluid loss. These studies can be linked with other animal studies which indicate that within the first 12 h of life, renal vascular resistance falls by 50% (1.03 mmHg/ml/min to 0.5 mmHg/ml/min) (Gruskin et al, 1970; Aschinberg et al, 1975). This finding challenges the theory that intrarenal shunts close after birth and, as PI is related to peripheral vascular resistance (Evans et al, 1980; Skidmore et al, 1980), correlates well with our observations. The appearance of the normal renal artery Doppler signal has been likened to a ski-slope. Its characteristics are those of a low-impedance vessel with continuous forward flow throughout diastole. Various diseases alter the resistance to flow through vessels either directly or indirectly. Attempts have been made to correlate measurements of these changes with the disease states. Most reports concentrate on Pourcelot's resistance index (PI) and the pulsatility index of Gosling (Nelson & Pretorius, 1988). Changes in the PI on Doppler studies should be readily detectable and if direct evidence of alteration to renal blood flow in high-risk infants can be made available, this would be extremely valuable (Daniel & James, 1976). Duplex Doppler ultrasound of the renal arteries offers a non-invasive method for investigation of the blood supply to the kidney in the infant. It is important
Figure 4. Pourcelot's index plotted against the age of the infant in hours. The fitted trend is shown. Right kidney (O); left
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A. C. Lamont, H. S. Hall, J. R. Thompson and D. H. Evans
for the better understanding of the role played by disturbances in blood supply to the kidney and it may help in the monitoring of therapy.
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Acknowledgments The authors would like to thank the staff of the Obstetric Department of the Leicester Royal Infirmary for access to their patients and for assistance during the research period, Dr E. Merk for translation and Dr J. Pelmore for help and valuable discussion.
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The British Journal of Radiology, May 1991